Assembly of a 40 Mb Eukaryotic Genome from Short Sequence Reads: , a Model Organism for Fungal Morphogenesis
Filamentous fungi are of great importance in ecology, agriculture, medicine, and biotechnology. Thus, it is not surprising that genomes for more than 100 filamentous fungi have been sequenced, most of them by Sanger sequencing. While next-generation sequencing techniques have revolutionized genome resequencing, e.g. for strain comparisons, genetic mapping, or transcriptome and ChIP analyses, de novo assembly of eukaryotic genomes still presents significant hurdles, because of their large size and stretches of repetitive sequences. Filamentous fungi contain few repetitive regions in their 30–90 Mb genomes and thus are suitable candidates to test de novo genome assembly from short sequence reads. Here, we present a high-quality draft sequence of the Sordaria macrospora genome that was obtained by a combination of Illumina/Solexa and Roche/454 sequencing. Paired-end Solexa sequencing of genomic DNA to 85-fold coverage and an additional 10-fold coverage by single-end 454 sequencing resulted in ∼4 Gb of DNA sequence. Reads were assembled to a 40 Mb draft version (N50 of 117 kb) with the Velvet assembler. Comparative analysis with Neurospora genomes increased the N50 to 498 kb. The S. macrospora genome contains even fewer repeat regions than its closest sequenced relative, Neurospora crassa. Comparison with genomes of other fungi showed that S. macrospora, a model organism for morphogenesis and meiosis, harbors duplications of several genes involved in self/nonself-recognition. Furthermore, S. macrospora contains more polyketide biosynthesis genes than N. crassa. Phylogenetic analyses suggest that some of these genes may have been acquired by horizontal gene transfer from a distantly related ascomycete group. Our study shows that, for typical filamentous fungi, de novo assembly of genomes from short sequence reads alone is feasible, that a mixture of Solexa and 454 sequencing substantially improves the assembly, and that the resulting data can be used for comparative studies to address basic questions of fungal biology.
Vyšlo v časopise:
Assembly of a 40 Mb Eukaryotic Genome from Short Sequence Reads: , a Model Organism for Fungal Morphogenesis. PLoS Genet 6(4): e32767. doi:10.1371/journal.pgen.1000891
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Research Article
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https://doi.org/10.1371/journal.pgen.1000891
Souhrn
Filamentous fungi are of great importance in ecology, agriculture, medicine, and biotechnology. Thus, it is not surprising that genomes for more than 100 filamentous fungi have been sequenced, most of them by Sanger sequencing. While next-generation sequencing techniques have revolutionized genome resequencing, e.g. for strain comparisons, genetic mapping, or transcriptome and ChIP analyses, de novo assembly of eukaryotic genomes still presents significant hurdles, because of their large size and stretches of repetitive sequences. Filamentous fungi contain few repetitive regions in their 30–90 Mb genomes and thus are suitable candidates to test de novo genome assembly from short sequence reads. Here, we present a high-quality draft sequence of the Sordaria macrospora genome that was obtained by a combination of Illumina/Solexa and Roche/454 sequencing. Paired-end Solexa sequencing of genomic DNA to 85-fold coverage and an additional 10-fold coverage by single-end 454 sequencing resulted in ∼4 Gb of DNA sequence. Reads were assembled to a 40 Mb draft version (N50 of 117 kb) with the Velvet assembler. Comparative analysis with Neurospora genomes increased the N50 to 498 kb. The S. macrospora genome contains even fewer repeat regions than its closest sequenced relative, Neurospora crassa. Comparison with genomes of other fungi showed that S. macrospora, a model organism for morphogenesis and meiosis, harbors duplications of several genes involved in self/nonself-recognition. Furthermore, S. macrospora contains more polyketide biosynthesis genes than N. crassa. Phylogenetic analyses suggest that some of these genes may have been acquired by horizontal gene transfer from a distantly related ascomycete group. Our study shows that, for typical filamentous fungi, de novo assembly of genomes from short sequence reads alone is feasible, that a mixture of Solexa and 454 sequencing substantially improves the assembly, and that the resulting data can be used for comparative studies to address basic questions of fungal biology.
Zdroje
1. HawksworthDL
2001 The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol Res 105 1422 1432
2. StajichJE
BerbeeML
BlackwellM
HibbettDS
JamesTY
2009 The fungi. Curr Biol 19 R840 R845
3. BuckleyM
2008 The fungal kingdom - diverse and essential roles in earth's ecosystem Washington DC American Academy of Microbiology
4. SmithSE
ReadDJ
2000 Mycorrhizal symbiosis London, San Diego Academic Press
5. ArcherDB
ConnertonIF
MacKenzieDA
2008 Filamentous fungi for production of food additives and processing aids. Adv Biochem Eng Biotechnol 111 99 147
6. HoffmeisterD
KellerNP
2007 Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep 24 393 416
7. GoffeauA
BarrellBG
BusseyH
DavisRW
DujonB
1996 Life with 6000 genes. Science 274 546 567
8. ShendureJ
LiH
2008 Next-generation DNA sequencing. Nature Biotechnol 26 1135 1145
9. WhitefordN
HaslamN
WeberG
Prügel-BennettA
EssexJW
2005 An analysis of the feasibility of short read sequencing. Nucl Acids Res 33 e171
10. MarguliesM
EgholmM
AltmanWE
AttiyaS
BaderJS
2005 Genome sequencing in microfabricated high-density picolitre reactors. Nature 437 376 380
11. ReinhardtJA
BaltrusDA
NishimuraMT
JeckWR
JonesCD
2009 De novo assembly using low-coverage short read sequence data from the rice pathogen Pseudomonas syringae pv. oryzae. Genome Res 19 294 305
12. DiGuistiniS
LiaoN
PlattD
RobertsonG
SeidelM
2009 De novo genome sequence assembly of a filamentous fungus using Sanger, 454 and Illumina sequence data. Genome Biol 10 R94
13. LiR
FanW
TianG
ZhuH
HeL
2009 The sequence and de novo assembly of the giant panda genome. Nature advance online publication doi:10.1038/nature08696
14. KückU
PöggelerS
NowrousianM
NoltingN
EnghI
2009 Sordaria macrospora, a model system for fungal development.
AnkeT
WeberD
The Mycota XV, Physiology and Genetics. 1st ed Berlin, Heidelberg Springer 17 39
15. ZicklerD
2005 Meiosis in mycelial fungi.
KüesU
FischerR
The Mycota I Growth, differentiation and sexuality Berlin, Heidelberg Springer 415 438
16. ZicklerD
2006 From early homologue recognition to synaptonemal complex formation. Chromosoma 115 158 174
17. PöggelerS
NowrousianM
KückU
2006 Fruiting-body development in ascomycetes.
KüesU
FischerR
The Mycota I Berlin, Heidelberg Springer 325 355
18. EsserK
StraubJ
1958 Genetische Untersuchungen an Sordaria macrospora Auersw., Kompensation und Induktion bei genbedingten Entwicklungsdefekten. Z Vererbungsl 98 729 746
19. NowrousianM
RingelbergC
DunlapJC
LorosJJ
KückU
2005 Cross-species microarray hybridization to identify developmentally regulated genes in the filamentous fungus Sordaria macrospora. Mol Genet Genomics 273 137 149
20. PöggelerS
KückU
2006 Highly efficient generation of signal transduction knockout mutants using a fungal strain deficient in the mammalian ku70 ortholog. Gene 378 1 10
21. PöggelerS
MasloffS
HoffB
MayrhoferS
KückU
2003 Versatile EGFP reporter plasmids for cellular localization of recombinant gene products in filamentous fungi. Curr Genet 43 54 61
22. PöggelerS
NowrousianM
JacobsenS
KückU
1997 An efficient procedure to isolate fungal genes from an indexed cosmid library. J Microbiol Meth 29 49 61
23. RechC
EnghI
KückU
2007 Detection of hyphal fusion in filamentous fungi using differently fluorescene-labeled histones. Curr Genet 52 259 266
24. WalzM
KückU
1995 Transformation of Sordaria macrospora to hygromycin B resistance: characterization of transformants by electrophoretic karyotyping and tetrad analysis. Curr Genet 29 88 95
25. EnghI
WürtzC
Witzel-SchlömpK
ZhangHY
HoffB
2007 The WW domain protein PRO40 is required for fungal fertility and associates with Woronin bodies
26. MasloffS
PöggelerS
KückU
1999 The pro1+ gene from Sordaria macrospora encodes a C6 zinc finger transcription factor required for fruiting body development. Genetics 152 191 199
27. NowrousianM
FrankS
KoersS
StrauchP
WeitnerT
2007 The novel ER membrane protein PRO41 is essential for sexual development in the filamentous fungus Sordaria macrospora. Mol Microbiol 64 923 937
28. PöggelerS
KückU
2004 A WD40 repeat protein regulates fungal cell differentiation and can be replaced functionally by the mammalian homologue striatin. Eukaryot Cell 3 232 240
29. StorlazziA
TesséS
GarganoS
JamesF
KlecknerN
2003 Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division. Genes Dev 17 2675 2687
30. StorlazziA
TesseS
Ruprich-RobertG
GarganoS
PöggelerS
2008 Coupling meiotic chromosome axis integrity to recombination. Genes Dev 22 796 809
31. van HeemstD
JamesF
PöggelerS
Berteaux-LecellierV
ZicklerD
1999 Spo76p is a conserved chromosome morphogenesis protein that links the mitotic and meiotic programs. Cell 98 261 271
32. NowrousianM
MasloffS
PöggelerS
KückU
1999 Cell differentiation during sexual development of the fungus Sordaria macrospora requires ATP citrate lyase activity. Mol Cell Biol 19 450 460
33. McClintockB
1945 Neurospora. I. Preliminary observations of the chromosomes of Neurospora crassa. Am J Bot 32 671 678
34. OrbachM
VollrathD
DavisRW
YanofskyC
1988 An electrophoretic karyotype of Neurospora crassa. Mol Cell Biol 8 1469 1473
35. PöggelerS
MasloffS
JacobsenS
KückU
2000 Karyotype polymorphism correlates with intraspecific infertility in the homothallic ascomycete Sordaria macrospora. J Evol Biol 13 281 289
36. NowrousianM
2009 A novel polyketide biosynthesis gene cluster is involved in fruiting body morphogenesis in the filamentous fungi Sordaria macrospora and Neurospora crassa. Curr Genet 55 185 198
37. NowrousianM
WürtzC
PöggelerS
KückU
2004 Comparative sequence analysis of Sordaria macrospora and Neurospora crassa as a means to improve genome annotation. Fungal Genet Biol 41 285 292
38. EsserK
1982 Cryptogams - Cyanobacteria, Algae, Fungi, Lichens London Cambridge University Press
39. PerkinsDD
1992 Neurospora: the organism behind the molecular revolution. Genetics 130 687 701
40. JacobsonDJ
DettmanJR
AdamsRI
BoeslC
SultanaS
2006 New findings of Neurospora in Europe and comparisons of diversity in temperate climates on continental scales. Mycologia 98 550 559
41. JacobsonDJ
PowellAJ
DettmanJR
SaenzGS
BartonMM
2004 Neurospora in temperate forests of western North America. Mycologia 96 66 74
42. ZerbinoDR
BirneyE
2008 Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18 821 829
43. GalaganJE
CalvoSE
BorkovichKA
SelkerEU
ReadND
2003 The genome sequence of the filamentous fungus Neurospora crassa. Nature 422 859 868
44. DeweyCN
2007 Aligning multiple whole genomes with Mercator and MAVID.
BergmanNH
Comparative genomics Totowa Humana Press
45. LiuQ
MackeyAJ
RoosDS
PereiraFCN
2008 Evigan: a hidden variable model for integrating gene evidence for eukaryotic gene predictions. Bioinformatics 24 597 605
46. BranscombE
PredkiP
2002 On the high value of low standards. J Bacteriol 194 6406 6409
47. FraserCM
EisenJA
NelsonKE
PaulsenIT
SalzbergSL
2002 The value of complete microbial genome sequencing (you get what you pay for). J Bacteriol 184 6403 6405
48. KasugaT
MannhauptG
GlassNL
2009 Relationship between phylogenetic distribution and genomic features in Neurospora crassa. PLOS ONE 4 e5286 doi:10.1371/journal.pone.0005286
49. EddySR
1998 Profile Hidden Markov Models. Bioinformatics 14 755 763
50. FinnRD
TateJ
MistryJ
CoggillPC
SammutSJ
2008 The Pfam protein families database. Nucl Acids Res 36 D281 288
51. ConesaA
GotzS
Garcia-GomezJM
TerolJ
TalonM
2005 Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21 3674 3676
52. ZdobnovEM
ApweilerR
2001 InterProScan - an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17 847 848
53. LiL
StoeckertCJJ
RoosDS
2003 OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Res 13 2178 2189
54. JurkaJ
1998 Repeats in genomic DNA: mining and meaning. Curr Opin Struct Biol 8 333 337
55. SchnablePS
WareD
FultonRS
SteinJC
WeiF
2009 The B73 maize genome: complexity, diversity, and dynamics. Science 326 1112 1115
56. LynchM
2007 The origins of genome architecture Sunderland, MA Sinauer Assocs. Inc
57. KempkenF
KückU
1998 Transposons in filamentous fungi - facts and perspectives. Bioessays 20 652 659
58. BraumannI
van den BergM
KempkenF
2007 Transposons in biotechnologically relevant strains of Aspergillus niger and Penicillium chrysogenum. Fungal Genet Biol 44 1399 1414
59. KapitonovVV
JurkaJ
2008 A universal classification of eukaryotic transposable elements in Repbase. Nat Rev Genet 9 411 412
60. KinseyJ
HelberJ
1989 Isolation of a transposable element from Neurospora crassa. Proc Nat Acad Sci USA 86 1929 1933
61. KempkenF
WindhoferF
2001 The hAT family: a versatile transposon group common to plants, fungi, animals, and man. Chromosoma 110 1 9
62. DaboussiMJ
Langint
BrygooY
1992 Fot1, a new family of fungal transposable elements. Mol Gen Genet 232 12 16
63. CuomoCA
GüldenerU
XuJR
TrailF
TurgeonBG
2007 The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317 1400 1402
64. DeanRA
TalbotNJ
EbboleDJ
FarmanML
MitchellTK
2005 The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434 980 986
65. BraumannI
van den BergM
KempkenF
2008 Strain-specific retrotransposon-mediated recombination in a commercially used Aspergillus niger strain. Mol Genet Genomics 280 319 325
66. RasmussenJP
TaylorAH
MaLJ
PurcellS
KempkenF
2004 Guest, a transposable element belonging to the Tc1/mariner superfamily is an ancient invader of Neurospora genomes. Fungal Genet Biol 41 52 61
67. GraiaF
LespinetO
RimbaultB
Dequard-ChablatM
CoppinE
2001 Genome quality control: RIP (repeat-induced point mutation) comes to Podospora. Mol Microbiol 40 586 595
68. HamannA
FellerF
OsiewaczHD
2000 The degenerate DNA transposon Pat and repeat-induced point mutation (RIP) in Podospora anserina. Mol Gen Genet 263 1061 1069
69. IkedaK
NakayashikiH
KataokaT
TambaH
HashimotoY
2002 Repeat-induced point mutation (RIP) in Magnaporthe grisea: implications for its sexual cycle in the natural field context. Mol Microbiol 45 1355 1364
70. IdnurmA
HowlettBJ
2003 Analysis of loss of pathogenicity mutants reveals that repeat-induced point mutations can occur in the Dothideomycete Leptosphaeria maculans. Fungal Genet Biol 39 31 37
71. GalaganJE
SelkerEU
2004 RIP: the evolutionary cost of genome defense. Trends Genet 20 417 423
72. MargolinBS
Garrett-EngelePW
StevensJN
FritzDY
Garrett-EngeleC
1998 A methylated Neurospora 5S rRNA pseudogene contains a transposable element inactivated by repeat-induced point mutation. Genetics 149 1787 1797
73. FreitagM
WilliamsRL
KotheGO
SelkerEU
2002 A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc Nat Acad Sci USA 99 8802 8807
74. MalagnacF
WendelB
GoyonC
FaugeronG
ZicklerD
1997 A gene essential for de novo methylation and development in Ascobolus reveals a novel type of eukaryotic DNA methyltransferase structure. Cell 91 281 290
75. LeeDW
FreitagM
SelkerEU
AramayoR
2008 A cytosine methyltransferase homologue is essential for sexual development in Aspergillus nidulans. PLoS ONE 3 e2531 doi:10.1371/journal.pone.0002531
76. FulciV
MacinoG
2007 Quelling: post-transcriptional gene silencing guided by small RNAs in Neurospora crassa. Curr Opin Microbiol 10 199 203
77. ShiuPKT
RajuNB
ZicklerD
MetzenbergRL
2001 Meiotic silencing by unpaired DNA. Cell 107 905 916
78. EnghI
NowrousianM
KückU
2007 Regulation of melain biosynthesis via the dihydroxynaphtalene pathway is dependent on sexual development in the ascomycete Sordaria macrospora. FEMS Microbiol Lett 275 62 70
79. NowrousianM
PiotrowskiM
KückU
2007 Multiple layers of temporal and spatial control regulate accumulation of the fruiting body-specific protein APP in Sordaria macrospora and Neurospora crassa. Fungal Genet Biol 44 602 614
80. KückU
2005 A Sordaria macrospora mutant lacking the leu1 gene shows a developmental arrest during fruiting body formation. Mol Genet Genomics 274 307 315
81. BorkovichKA
AlexLA
YardenO
FreitagM
TurnerGE
2004 Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68 1 108
82. ZicklerD
2009 Observing meiosis in filamentous fungi: Sordaria and Neurospora. Methods Mol Biol 558 91 114
83. NowrousianM
KückU
2006 Comparative gene expression analysis of fruiting body development in two filamentous fungi. FEMS Microbiol Lett 257 328 335
84. HardingRW
MellesS
1983 Genetic analysis of phototropism of Neurospora crassa perithecial beaks using white collar and albino mutants. Plant Physiol 72 996 1000
85. ReadND
1983 A scanning electron microscopic study of the external features of perithecium development in Sordaria humana. Can J Bot 61 3217 3229
86. FroehlichAC
LiuY
LorosJJ
DunlapJC
2002 White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297 815 819
87. HeQ
ChengP
YangY
WangL
GardnerK
2002 White collar-1, a DNA binding transcription factor and a light sensor. Science 297 840 843
88. BallarioP
VittoriosoP
MagrelliA
TaloraC
CabibboA
1996 White collar-1, a central regulator of blue-light responses in Neurospora, is a zinc finger protein. EMBO J 15 1650 1657
89. PurschwitzJ
MüllerS
KastnerC
SchöserM
HaasH
2008 Functional and physical interaction of blue- and red-light sensors in Aspergillus nidulans. Curr Biol 18 255 259
90. BlumensteinA
VienkenK
TaslerR
PurschwitzJ
VeithD
2005 The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Current Biology 15 1833 1838
91. LindenH
BallarioP
ArpaiaG
MacinoG
1999 Seeing the light: News in Neurospora blue light signal transduction. Adv Genet 41 35 54
92. BieszkeJA
SpudichEN
ScottKL
BorkovichKA
SpudichJL
1999 A eukaryotic protein, NOP-1, binds retinal to form an archaeal rhodopsin-like photochemically reactive pigment. Biochemistry 38 14138 14145
93. GriffithsAJ
1992 Fungal senescence. Annu Rev Genet 26 351 372
94. OsiewaczHD
1990 Molecular analysis of aging processes in fungi. Mut Res 237 1 8
95. WuM
XuL-G
LiX
ZhaiZ
ShuH-B
2002 AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis. J Biol Chem 277 25617 25623
96. AverbeckNB
JensenON
MannM
SchäggerH
OsiewaczHD
2000 Identification and characterization of PaMTH1, a putative O-methyltransferase accumulating during senescence of Podospora anserina cultures. Curr Genet 37 200 208
97. GroebeK
KrauseF
KunstmannB
UnterluggauerH
ReifschneiderNH
2007 Differential proteomic profiling of mitochondria from Podospora anserina, rat and human reveals distinct patterns of age-related oxidative changes. Exp Gerontol 42 887 898
98. KunstmannB
OsiewaczHD
2008 Over-expression of an S-adenosylmethionine-dependent methyltransferase leads to an extended lifespan of Podospora anserina without impairments in vital functions. Aging Cell 7 651 662
99. KunstmannB
OsiewaczHD
2009 The S-adenosylmethionine dependent O-methyltransferase PaMTH1: a longevity assurance factor protecting Podospora anserina against oxidative stress. Aging 1 328 334
100. MataJ
LyneR
BurnsG
BählerJ
2002 The transcriptional program of meiosis and sporulation in fission yeast. Nat Genet 32 143 147
101. SchlechtU
PrimigM
2003 Mining meiosis and gametogenesis with DNA microarrays. Reproduction 225 447 456
102. EspagneE
LespinetO
MalagnacF
Da SilvaC
JaillonO
2008 The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol 9 R77
103. PageSL
HawleyRS
2004 The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20 525 558
104. MalikSB
PightlingAW
StefaniakLM
SchurkoAM
LogsdonJMJ
2008 An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis. PLOS ONE 3 e2879 doi:10.1371/journal.pone.0002879
105. HunterN
2006 Meiotic recombination.
AguileraA
RothsteinR
Molecular genetics of recombination Berlin, Heidelberg Springer 381 443
106. O'GormanCM
FullerHT
DyerPS
2009 Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457 471 475
107. PöggelerS
2002 Genomic evidence for mating abilities in the asexual pathogen Aspergillus fumigatus. Curr Genet 42 153 160
108. ReadND
FleissnerA
RocaMG
GlassNL
2010 Hyphal fusion.
BorkovichKA
EbboleD
Molecular biology of filamentous fungi Am. Soc. Microbiol 260 273
109. SaupeS
2000 Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiol Mol Biol Rev 64 489 502
110. MicaliOC
SmithML
2006 A nonself recognition gene complex in Neurospora crassa. Genetics 173 1991 2004
111. CortesiP
McCullochCE
SongH
LinH
MilgroomMG
2001 Genetic control of horizontal virus transmission in the chestnut blight fungus, Cryphonectria parasitica. Genetics 159 107 118
112. DebetsA
GriffithsAJ
1998 Poymorphism of het genes prevents resource plundering in Neurospora crassa. Mycol Res 102 1343 1349
113. DebetsF
YangX
GriffithsAJ
1994 Vegetative incompatibility in Neurospora: its effect on horizontal transfer of mitochondrial plasmids and senescence in natural populations. Curr Genet 26 113 119
114. van DiepeningenAD
DebetsAJ
HoekstraRF
1997 Heterokaryon incompatibility blocks virus transfer among natural isolates of black Aspergilli. Curr Genet 32 209 217
115. GlassNL
KanekoI
2003 Fatal attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryot Cell 2 1 8
116. SmithML
MicaliOC
HubbardSP
Mir-RashedN
JacobsonDJ
2000 Vegetative incompatibility in the het-6 region of Neurospora crassa is mediated by two linked genes. Genetics 155 1095 1104
117. PaolettiM
SaupeSJ
ClavéC
2007 Genesis of a fungal non-self recognition repertoire. PLoS ONE 2 e283 doi:10.1371/journal.pone.0000283
118. BeadleGW
CoonradtVL
1944 Heterocaryosis in Neurospora crassa. Genetics 29 291 308
119. EspagneE
BalhadèreP
PeninML
BarreauC
TurcqB
2002 HET-E and HET-D belong to a new subfamily of WD40 proteins involved in vegetative incompatibility specificity in the fungus Podospora anserina. Genetics 161 71 81
120. ShiuPK
GlassNL
1999 Molecular characterization of tol, a mediator of mating-type-associated vegetative incompatibility in Neurospora crassa. Genetics 151 545 555
121. FedorovaN
BadgerJ
RobsonG
WortmanJ
NiermanW
2005 Comparative analysis of programmed cell death pathways in filamentous fungi. BMC Genomics 6 177
122. KanekoI
DementhonK
XiangQ
GlassNL
2006 Nonallelic interactions between het-c and a polymorphic locus, pin-c, are essential for nonself recognition and programmed cell death in Neurospora crassa. Genetics 172 1545 1555
123. SarkarS
IyerG
WuJ
GlassNL
2002 Nonself recognition is mediated by HET-C heterocomplex formation during vegetative incompatibility. EMBO J 21 4841 4850
124. JacobsonDJ
BeurkensK
KlomarensKL
1998 Microscopic and ultrastructural examination of vegetative incompatibility in partial diploids heterozygous at het loci in Neurospora crassa. Fungal Genet Biol 23 45 56
125. MylekOM
1975 Heterokaryon incompatibility genes in Neurospora crassa detected using duplication-producing chromosome rearrangements. Genetics 80 107 124
126. PerkinsDD
1975 The use of duplication-generating rearrangements for studying heterokaryon incompatibility genes in Neurospora. Genetics 80 87 105
127. WuJ
GlassNL
2001 Identification of specificity determinants and generation of alleles with novel specificity at the het-c heterokaryon incompatibility locus of Neurospora crassa. Mol Cell Biol 21 1045 1057
128. PöggelerS
RischS
KückU
OsiewaczHD
1997 Mating-type genes from the homothallic fungus Sordaria macrospora are functionally expressed in a heterothallic ascomycete. Genetics 147 567 580
129. JacobsonDJ
1992 Control of mating type heterokaryon incompatibility by the tol gene in Neurospora crassa and N. tetrasperma. Genome 35 347 353
130. Mir-RashedN
JacobsonDJ
DehghanyMR
MicaliOC
SmithML
2000 Molecular and functional analyses of incompatibility genes at het-6 in a population of Neurospora crassa. Fungal Genet Biol 30 197 205
131. PowellAJ
JacobsonDJ
NatvigDO
2007 Ancestral polymorphism and linkage disequilibrium at the het-6 region in pseudohomothallic Neurospora tetrasperma. Fungal Genet Biol 44 896 904
132. CoxRJ
2007 Polyketides, proteins and genes in fungi: programmed nano-machines begin to reveal their secrets. Org Biomol Chem 5 2010 2026
133. WalshCT
2004 Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303 1805 1810
134. KellerNP
HohnTM
1997 Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol 21 17 29
135. KrokenS
GlassNL
TaylorJW
YoderOC
TurgeonBG
2003 Phylogenomic analyis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Nat Acad Sci USA 100 15670 15675
136. HaneJK
LoweRGT
SolomonPS
TanK-C
SchochCL
2007 Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19 3347 3368
137. RosewichUL
KistlerHC
2000 Role of horizontal gene transfer in the evolution of fungi. Annu Rev Phytopathol 38 326 363
138. KhaldiN
WolfeKH
2008 Elusive origins of the extra genes in Aspergillus oryzae. PLOS ONE 3 e3036 doi:10.1371/journal.pone.0003036
139. PatronNJ
WallerRF
CozijnsenAJ
StraneyDC
GardinerDM
2007 Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes. BMC Evol Biol 7 174
140. KhaldiN
CollemareJ
LebrunM-H
WolfeKH
2008 Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol 9 R18
141. FriesenTL
StukenbrockEH
LiuZ
MeinhardtS
LingH
2006 Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38 953 956
142. FedorovaND
KhaldiN
JoardarVS
MaitiR
AmedeoP
2008 Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLOS Genet 4 e1000046 doi:10.1371/journal.pgen.1000046
143. Garcia-VallvéS
RomeuA
PalauJ
2000 Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol Biol Evol 17 352 361
144. ColemanJJ
RounsleySD
Rodriguez-CarresM
KuoA
WasmannCC
2009 The genome of Nectria haematococca: Contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5 e1000618 doi:10.1371/journal.pgen.1000618
145. HogeJHC
SpringerJ
ZantingeB
WesselsJGH
1982 Absence of differences in polysomal RNAs from vegetative monokaryotic and dikaryotic cells of the fungus Schizophyllum commune. Exp Mycol 6 225 232
146. PomraningKR
SmithKM
FreitagM
2009 Genome-wide high throughput analysis of DNA methylation in eukaryotes. Methods 47 142 150
147. AltschulSF
MaddenTL
SchafferAA
ZhangJ
ZhangZ
1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389 3402
148. EngelsR
YuT
BurgeC
MesirovJP
DeCaprioD
2006 Combo: a whole genome comparative browser. Bioinformatics 22 1782 1783
149. KorfI
2004 Gene finding in novel genomes. BMC Bioinformatics 5 59
150. StankeM
SchöffmannO
MorgensternB
WaackS
2006 Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics 7 62
151. StankeM
WaackS
2003 Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19 suppl. 2 ii215 225
152. BesemerJ
BorodovskyM
2005 GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucl Acids Res 33 W451 454
153. BirneyE
ClampM
DurbinR
2004 GeneWise and Genomewise. Genome Res 14 988 955
154. StajichJE
BlockD
BoulezK
BrennerSE
ChervitzSA
2002 The Bioperl Toolkit: Perl modules for the life sciences. Genome Res 12 1611 1618
155. HortonP
ParkKJ
ObayashiT
NakaiK
2006 Protein subcellular localization prediction with WoLF PSORT. 39 48 Proceedings of the 4th Annual Asia Pacific Bioinformatics Conference APBC06, Taipei, Taiwan
156. BendtsenJD
NielsenH
von HeijneG
BrunakS
2004 Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340 783 795
157. TusnadyGE
SimonI
1998 Principles governing amino acid composition of integral membrane proteins: Applications to topology prediction. J Mol Biol 283 489 506
158. KroghA
LarssonB
von HeijneG
SonnhammerELL
2001 Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol 305 567 580
159. LoweTM
EddySR
1997 tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucl Acids Res 25 955 964
160. NawrockiEP
KolbeDL
EddySR
2009 Infernal 1.0: inference of RNA alignments. Bioinformatics 25 1335 1337
161. TaquistH
CuiY
ArdellDH
2007 TFAM 1.0: an online tRNA function classifier. Nucl Acids Res 35 W350 353
162. NowrousianM
CebulaP
2005 The gene for a lectin-like protein is transcriptionally activated during sexual development, but is not essential for fruiting body formation in the filamentous fungus Sordaria macrospora. BMC Microbiol 5 64
163. ThompsonJD
GibsonTJ
PlewniakF
JeanmouginF
HigginsDG
1997 The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24 4876 4882
164. WaterhouseAM
ProcterJB
MartinDMA
ClampM
BartonGJ
2009 Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25 1189 1191
165. HuelsenbeckJP
RonquistF
2001 Bayesian inference of phylogeny. Bioinformatics 17 754 755
166. RonquistF
HuelsenbeckJP
2003 Bayesian phylogenetic inference under mixed models. Bioinformatics 19 1572 1574
167. HallBG
2004 Phylogenetic trees made easy Sunderland Sinauer Associates
168. HusonDH
RichterDC
RauschC
DezulianT
FranzM
2007 Dendroscope - An interactive viewer for large phylogenetic trees. BMC Bioinformatics 8 460
169. PageR
1996 TREEVIEW: an application to display phylogenetic trees on personal computers. Appl Biosci 12 357 358
170. DementhonK
IyerG
GlassNL
2006 VIB-1 Is required for expression of genes necessary for programmed cell death in Neurospora crassa. Eukaryot Cell 5 2161 2173
171. LiuYJ
HallBD
2004 Body plan evolution of ascomycetes, as inferred from an RNA polymerase II phylogeny. Proc Nat Acad Sci USA 101 4507 4512
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 4
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